bs_bs_banner Botanical Journal of the Linnean Society, 2013, 171, 225–243. With 5 figures Molecular phylogenetics and biogeography of Neotropical Paepalanthoideae with emphasis on Brazilian Paepalanthus (Eriocaulaceae) Downloaded from https://academic.oup.com/botlinnean/article-abstract/171/1/225/2557485 by guest on 06 January 2020 MARCELO TROVÓ1,2*, MARIA JOSÉ GOMES DE ANDRADE3, PAULO TAKEO SANO1, PATRÍCIA LUZ RIBEIRO3 and CÁSSIO VAN DEN BERG3 1Laboratório de Sistemática Vegetal, Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, Rua do Matão 277, Cidade Universitária, CEP 05508-900, São Paulo, Brazil 2Evolution and Biodiversity of Plants, Faculty for Biology and Biotechnology, Ruhr University Bochum, D-44780 Bochum, Germany 3Laboratório de Sistemática Molecular de Plantas, Departamento de Ciências Biológicas, Universidade Estadual de Feira de Santana, Av. Transnordestina s.n., CEP 44036-900, Feira de Santana, Brazil Received 10 January 2012; revised 25 June 2012; accepted for publication 29 August 2012 Subfamily Paepalanthoideae encompass the largest generic diversity in Eriocaulaceae. In the present study, the main goals were to infer the phylogeny of this subfamily focusing on Paepalanthus, to evaluate recent classifica- tions and morphological characters in a phylogenetic context and to reconstruct the historical biogeography of the group. Sampling involved 94 ingroup species corresponding to all recognized genera and three outgroup species. Two molecular data sets, nuclear ribosomal internal transcribed spacer (nrITS) and plastid trnL-trnF, were analysed under parsimony and Bayesian methods. Rondonanthus is monophyletic and confirmed as sister to the remaining Paepalanthoideae. Leiothrix and Actinocephalus are each monophyletic, whereas Syngonanthus may be either monophyletic or paraphyletic with the recognition of Philodice. Four subgenera of Paepalanthus are monophyletic, but P. subgenus Paepalanthus is polyphyletic. Morphological characters used in previous classifi- cations are assessed as putative synapomorphies for recognized genera. Some of the characters employed in defining Paepalanthus subcategories appear to have evolved multiple times, and many clades may be exclusively defined by molecular synapomorphies. Biogeographical reconstructions suggest that the current distribution patterns may be related to vicariance and a few long-distance dispersal events. Furthermore, some clades are restricted to narrow geographical areas, perhaps important as a means of conserving evolutionary processes. © 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 225–243. ADDITIONAL KEYWORDS: internal transcribed spacer (ITS) – morphology – South America – systematics – taxonomy – trnL-trnF. INTRODUCTION Hensold, 1990; Stützel, 1998; Sano, 2004; Parra et al., 2010; Andrade et al., 2011). The family is historically Eriocaulaceae comprise c. 1200 species and 11 genera divided into two subfamilies: Paepalanthoideae and distributed throughout the tropics (Giulietti & Eriocauloideae (Koernicke, 1863; Ruhland, 1903). The former is characterized as possessing haplostemonous *Corresponding author. Current address: Departamento de androecia, eglandular corollas and gynoecia with Botânica, Instituto de Biologia, Universidade Federal do Rio alternating stigmatic and nectariferous branches de Janeiro, CCS, Bloco A1, Cidade Universitária, Ilha do Fundão, CEP 21941-590, Rio de Janeiro, RJ, Brasil. E-mail: (Ruhland, 1903; Rosa & Scatena, 2007). All nine [email protected] genera and c. 800 species of Paepalanthoideae © 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 225–243 225 226 M. TROVÓ ET AL. (Fig. 1) are predominantly distributed throughout the Andrade, 2007; Andrade et al., 2010) was fairly Neotropics (Giulietti & Hensold, 1990; Stützel, 1998). similar: all confirming the monophyly of both sub- According to Giulietti et al. (2005), c. 95% of the families and the genera Leiothrix Ruhland and species included in this subfamily are narrow endem- Actinocephalus (Koern.) Sano emend. (F. N. Costa & ics and restricted to a few small populations. Some P. T. Sano, unpubl. data; including Paepalanthus sub- species are of great economic importance. Every section Aphorocaulon Ruhland) and the polyphyly of year, large numbers of inflorescences from species of Paepalanthus. Thus, based on the monophyly of Syngonanthus Ruhland, Comanthera L.B.Sm. and Paepalanthoideae (Giulietti et al., 1995; Unwin, 2004; Paepalanthus Mart. are exported to North America Andrade, 2007; Andrade et al., 2010), our main goal and Europe as ‘everlasting plants’ and, more recently, was to infer phylogenetic relationships in the sub- Downloaded from https://academic.oup.com/botlinnean/article-abstract/171/1/225/2557485 by guest on 06 January 2020 as ‘golden grass’ (Giulietti et al., 1988; Schmidt, family, with an emphasis on Paepalanthus and its Figueiredo & Scariot, 2007; Costa, Trovó & Sano, Brazilian subgroups. Evolution of morphological char- 2008; Parra et al., 2010). These species are not culti- acters and biogeographic history of the Paepalanthoi- vated but simply harvested in situ, leading to deple- deae were reconstructed in order to clarify the tion of the natural populations. Indeed, many species classification and evolution of the group in the of Paepalanthoideae are highly endangered. For Neotropics. example, 94 species have been cited on the Red List of State of Minas Gerais and 20 on the Red List of Brazil (Biodiversitas, 2008). Paepalanthus spp. are also MATERIAL AND METHODS notable for their antioxidant and mutagenic proper- TAXA SAMPLED ties (Varanda et al., 2006; Devienne et al., 2007). In Paepalanthoideae, Paepalanthus is the largest All nine genera of Paepalanthoideae and all infrage- genus with c. 380 species (Giulietti & Hensold, 1990; neric categories of Paepalanthus recognized by Stützel, 1998). Morphological and species diversity Ruhland (1903) were sampled, except for Paepalan- is concentrated in Brazilian campos rupestres in the thus subgenus Psilandra Ruhland, known exclusively Espinhaço Range and in the Guayana Shield High- from the type specimen. Overall, 94 species were lands (Giulietti & Hensold, 1990; Hensold, 1991, sampled as follows: Actinocephalus 5/28 (species 1999). The genus is characterized by pistillate sampled/species belonging to the genus), Comanthera flowers with free petals and stigmatic/nectariferous 3/37, Lachnocaulon Kunth 1/7, Leiothrix 6/64, Paepal- branches that are free at the same insertion point. anthus 73/~380, Philodice Mart. 1/2, Rondonanthus Nevertheless, with the exception of these few floral Herzog 2/6, Syngonanthus 2/~150 and Tonina Aubl. characters, morphological variation in both floral 1/1. The sampling in Paepalanthus and Syngonanthus and vegetative traits is broad. This variation pro- is limited at a first glance. However, many species of vided the basis for the proposition of > 20 infrage- these genera are known only from the type specimen neric categories in previous classifications of the or unknown type localities. Recent taxonomic revi- genus (Koernicke, 1863; Ruhland, 1903). Some cat- sions identified many synonyms in these groups, and egories, such as Paepalanthus subgenus Platycaulon the number of species of Paepalanthus and Syngo- Koern., are morphologically easily recognized, nanthus may actually be much smaller. Moreover, whereas others, such as Paepalanthus series Paepal- Syngonanthus is monomorphic in relation to the anthus, simply represent aggregations of possibly morphological traits evaluated (Koernicke, 1863; unrelated species (Stützel, 1998). Thus, the exten- Ruhland, 1903). Three species of Eriocaulon L. were sive morphological variation in Paepalanthus may included as outgroups, based on previous phylogenies obscure the phylogenetic relationships and explain, (Unwin, 2004; Andrade et al., 2010). The complete list at least in part, its complex nomenclatural and of taxa and voucher specimens is given in Appendix 1. taxonomic history. The first phylogenetic study involving Paepalan- thoideae was based entirely on morphological data SEQUENCES AND ALIGNMENT (Giulietti, Amaral & Bittrich, 1995). In this study, The nuclear internal transcribed spacer (ITS) region Paepalanthoideae emerged as monophyletic, whereas and the plastid trnL-trnF region were chosen because Paepalanthus was polyphyletic. In a later study, of their rate of sequence variation, based on previous Giulietti et al. (2000), taking into consideration mor- studies in the family by Unwin (2004), Andrade phology, anatomy and chemistry, concluded that (2007) and Andrade et al. (2010). Sequences for 59 Paepalanthoideae are paraphyletic, but many of the species were obtained from Andrade et al. (2010) and genera are monophyletic. Polyphyly of Paepalanthus additional sequences for 35 species were obtained for was also stated in that study. The outcome of recent this study. All GenBank accession numbers are listed molecular phylogenetic analyses (Unwin, 2004; in Appendix 1. © 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 225–243 EVOLUTION OF PAEPALANTHOIDEAE 227 Downloaded from https://academic.oup.com/botlinnean/article-abstract/171/1/225/2557485 by guest on 06 January 2020 Figure 1. Photographs of Paepalanthoideae representatives in nature. A, Actinocephalus polyanthus (Bong.) Sano. B, Comanthera linearis (Ruhland) L.R. Parra & Giul. C, Leiothrix crassifolia (Bong.) Ruhland. D, Paepalanthus chiquitensis